Trafficking of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPA) receptor subunit GluA2 from the endoplasmic reticulum is stimulated by a complex containing Ca2+/calmodulin-activated kinase II (CaMKII) and PICK1 protein and by release of Ca2+ from internal stores

Journal of Biological Chemistry

Volumn 289, Issue 27, 2014, Pages 19218-19230

  Lu, Wei ^a   Khatri, Latika ^a,b   Ziff, Edward B ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CELL MEMBRANES;

ACID RECEPTORS; CALCIUM DYNAMICS; CALCIUM RELEASE; ENDOPLASMIC RETICULUM; INTRACELLULAR CALCIUM; RATE-LIMITING STEPS; SIGNALING PATHWAYS;

CALMODULIN;

AMPA RECEPTOR; AMPA RECEPTOR SUBUNIT GLUA2; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; INOSITOL TRISPHOSPHATE; PROTEIN INTERACTING WITH PROTEIN KINASE C; RYANODINE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL MEMBRANE; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; EXPRESSION VECTOR; GENETIC TRANSFECTION; HELA CELL LINE; HIPPOCAMPAL NEURONAL CULTURE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TRAFFICKING; RAT;

BAR DOMAIN; CA2+/CALMODULIN-DEPENDENT PROTEIN KINASE II (CAMKII); CALCIUM; ENDOPLASMIC RETICULUM (ER); GLUA2; IONOTROPIC GLUTAMATE RECEPTOR; PICK1; TRAFFICKING; Α-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID RECEPTOR (AMPA RECEPTOR, AMPAR);

ANIMALS; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CARRIER PROTEINS; CELL LINE; CELL MEMBRANE; ENDOPLASMIC RETICULUM; FEEDBACK, PHYSIOLOGICAL; HIPPOCAMPUS; HUMANS; INOSITOL PHOSPHATES; NEURONS; NUCLEAR PROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; RECEPTORS, AMPA;

EID: 84903852162     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.511246     Document Type: Article

References (50)

1. Anggono, V., and Huganir, R. L. (2012) Regulation of AMPA receptor trafficking and synaptic plasticity. Curr. Opin. Neurobiol. 22, 461-469
2. Bredt, D. S., and Nicoll, R. A. (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40, 361-379
3. Malinow, R., and Malenka, R. C. (2002) AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103-126
4. Traynelis, S. F., Wollmuth, L. P., McBain, C. J., Menniti, F. S., Vance, K. M., Ogden, K. K., Hansen, K. B., Yuan, H., Myers, S. J., and Dingledine, R. (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 62, 405-496
5. Greger, I. H., Akamine, P., Khatri, L., and Ziff, E. B. (2006) Developmentally regulated, combinatorialRNAprocessing modulatesAMPAreceptor biogenesis. Neuron 51, 85-97
6. Greger, I. H., Khatri, L., Kong, X., and Ziff, E. B. (2003) AMPA receptor tetramerization is mediated by Q/R editing. Neuron 40, 763-774
7. Greger, I. H., Khatri, L., and Ziff, E. B. (2002) RNA editing at arg607 controls AMPA receptor exit from the endoplasmic reticulum. Neuron 34, 759-772
8. Hollmann, M., Hartley, M., and Heinemann, S. (1991) Ca2- permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252, 851-853
9. Burnashev, N., Monyer, H., Seeburg, P. H., and Sakmann, B. (1992) Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8, 189-198
10. Lu, W., Shi, Y., Jackson, A. C., Bjorgan, K., During, M. J., Sprengel, R., Seeburg, P. H., and Nicoll, R. A. (2009) Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62, 254-268
11. Wenthold, R. J., Petralia, R. S., Blahos, J., II, and Niedzielski, A. S. (1996) Evidence for multiple AMPA receptor complexes in hippocampal CA1/ CA2 neurons. J. Neurosci. 16, 1982-1989
12. Jia, Z., Agopyan, N., Miu, P., Xiong, Z., Henderson, J., Gerlai, R., Taverna, F. A., Velumian, A., MacDonald, J., Carlen, P., Abramow-Newerly, W., and Roder, J. (1996) Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron 17, 945-956
13. Shimshek, D. R., Jensen, V., Celikel, T., Geng, Y., Schupp, B., Bus, T., Mack, V., Marx, V., Hvalby, O., Seeburg, P. H., and Sprengel, R. (2006) Forebrainspecific glutamate receptor B deletion impairs spatial memory but not hippocampal field long-term potentiation. J. Neurosci. 26, 8428-8440
14. Jackson, A. C., and Nicoll, R. A. (2011) The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits. Neuron 70, 178-199
15. Barry, M. F., and Ziff, E. B. (2002) Receptor trafficking and the plasticity of excitatory synapses. Curr. Opin. Neurobiol. 12, 279-286
16. Shepherd, J. D., and Huganir, R. L. (2007) The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu. Rev. Cell Dev. Biol. 23, 613-643
17. Plant, K., Pelkey, K. A., Bortolotto, Z. A., Morita, D., Terashima, A., McBain, C. J., Collingridge, G. L., and Isaac, J. T. (2006) Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 9, 602-604
18. Lu, Y., Allen, M., Halt, A. R., Weisenhaus, M., Dallapiazza, R. F., Hall, D. D., Usachev, Y. M., McKnight, G. S., and Hell, J. W. (2007) Age-dependent requirement of AKAP150-anchored PKA and GluR2-lacking AMPA receptors in LTP. EMBO J. 26, 4879-4890
19. Adesnik, H., and Nicoll, R. A. (2007) Conservation of glutamate receptor 2-containing AMPA receptors during long-term potentiation. J. Neurosci. 27, 4598-4602
20. Liu, S. Q., and Cull-Candy, S. G. (2000) Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 405, 454-458
21. Gardner, S. M., Takamiya, K., Xia, J., Suh, J. G., Johnson, R., Yu, S., and Huganir, R. L. (2005) Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF. Neuron 45, 903-915
22. Liu, S. J., and Cull-Candy, S. G. (2005) Subunit interaction with PICK and GRIP controls Ca2- permeability of AMPARs at cerebellar synapses. Nat. Neurosci. 8, 768-775
23. Jackson, A. C., and Nicoll, R. A. (2011) Stargazin (TARP gamma-2) is required for compartment-specific AMPA receptor trafficking and synaptic plasticity in cerebellar stellate cells. J. Neurosci. 31, 3939-3952
24. Mameli, M., Balland, B., Luján, R., and Lüscher, C. (2007) Rapid synthesis and synaptic insertion of GluR2 for mGluR-LTD in the ventral tegmental area. Science 317, 530-533
25. Shi, S., Hayashi, Y., Esteban, J. A., and Malinow, R. (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105, 331-343
26. Granger, A. J., Shi, Y., Lu, W., Cerpas, M., and Nicoll, R. A. (2013) LTP requires a reserve pool of glutamate receptors independent of subunit type. Nature 493, 495-500
27. Osten, P., Khatri, L., Perez, J. L., Köhr, G., Giese, G., Daly, C., Schulz, T. W., Wensky, A., Lee, L. M., and Ziff, E. B. (2000) Mutagenesis reveals a role for ABP/GRIP binding to GluR2 in synaptic surface accumulation of the AMPA receptor. Neuron 27, 313-325
28. Perez, J. L., Khatri, L., Chang, C., Srivastava, S., Osten, P., and Ziff, E. B. (2001) PICK1 targets activated protein kinase C- to AMPA receptor clusters in spines of hippocampal neurons and reduces surface levels of the AMPA-type glutamate receptor subunit 2. J. Neurosci. 21, 5417-5428
29. Serulle, Y., Zhang, S., Ninan, I., Puzzo, D., McCarthy, M., Khatri, L., Arancio, O., and Ziff, E. B. (2007) A GluR1-cGKII interaction regulates AMPA receptor trafficking. Neuron 56, 670-688
30. Bardo, S., Cavazzini, M. G., and Emptage, N. (2006) The role of the endoplasmic reticulum Ca2- store in the plasticity of central neurons. Trends Pharmacol. Sci. 27, 78-84
31. Rose, C. R., and Konnerth, A. (2001) Stores not just for storage. intracellular calcium release and synaptic plasticity. Neuron 31, 519-522
32. Hanley, J. G., and Henley, J. M. (2005) PICK1 is a calcium-sensor for NMDA-induced AMPA receptor trafficking. EMBO J. 24, 3266-3278
33. Hanley, J. G. (2008) PICK1: a multi-talented modulator ofAMPAreceptor trafficking. Pharmacol. Ther. 118, 152-160
34. Xia, J., Zhang, X., Staudinger, J., and Huganir, R. L. (1999) Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron 22, 179-187
35. Citri, A., Bhattacharyya, S., Ma, C., Morishita, W., Fang, S., Rizo, J., and Malenka, R. C. (2010) Calcium binding to PICK1 is essential for the intracellular retention of AMPA receptors underlying long-term depression. J. Neurosci. 30, 16437-16452
36. Lu, W., and Ziff, E. B. (2005) PICK1 interacts with ABP/GRIP to regulate AMPA receptor trafficking. Neuron 47, 407-421
37. Chung, H. J., Xia, J., Scannevin, R. H., Zhang, X., and Huganir, R. L. (2000) Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. J. Neurosci. 20, 7258-7267
38. Matsuda, S., Mikawa, S., and Hirai, H. (1999) Phosphorylation of serine-880 in GluR2 by protein kinase C prevents its C terminus from binding with glutamate receptor-interacting protein. J. Neurochem. 73, 1765-1768
39. Brickey, D. A., Bann, J. G., Fong, Y. L., Perrino, L., Brennan, R. G., and Soderling, T. R. (1994) Mutational analysis of the autoinhibitory domain of calmodulin kinase II. J. Biol. Chem. 269, 29047-29054
40. Hudmon, A., and Schulman, H. (2002) Neuronal Ca2-/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function. Annu. Rev. Biochem. 71, 473-510
41. Lisman, J., Schulman, H., and Cline, H. (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci. 3, 175-190
42. Braun, A. P., and Schulman, H. (1995) A non-selective cation current activated via the multifunctional Ca2-calmodulin-dependent protein kinase in human epithelial cells. J. Physiol. 488, 37-55
43. Greger, I. H., Ziff, E. B., and Penn, A. C. (2007) Molecular determinants of AMPA receptor subunit assembly. Trends Neurosci. 30, 407-416
44. Hayashi, Y., Shi, S. H., Esteban, J. A., Piccini, A., Poncer, J. C., and Malinow, R. (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262-2267
45. Mansour, M., Nagarajan, N., Nehring, R. B., Clements, J. D., and Rosenmund, C. (2001) Heteromeric AMPA receptors assemble with a preferred subunit stoichiometry and spatial arrangement. Neuron 32, 841-853
46. Vandenberghe, W., Nicoll, R. A., and Bredt, D. S. (2005) Interaction with the unfolded protein response reveals a role for stargazin in biosynthetic AMPA receptor transport. J. Neurosci. 25, 1095-1102
47. Tomita, S., Stein, V., Stocker, T. J., Nicoll, R. A., and Bredt, D. S. (2005) Bidirectional synaptic plasticity regulated by phosphorylation of stargazin- like TARPs. Neuron 45, 269-277
48. Menuz, K., O'Brien, J. L., Karmizadegan, S., Bredt, D. S., and Nicoll, R. A. (2008) TARP redundancy is critical for maintainingAMPAreceptor function. J. Neurosci. 28, 8740-8746
49. Liu, S. J., and Zukin, R. S. (2007) Ca2-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci. 30, 126-134
50. Ménard, C., and Quirion, R. (2012) Group 1 metabotropic glutamate receptor function and its regulation of learning and memory in the aging brain. Front. Pharmacol. 3, 182